Int. Arch. . vol.19 número4

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Aspects of Oral Language, Speech, and Written

Language in Subjects with Temporal Lobe

Epilepsy of Dif

_ﬁ

cult Control

Ana Paula Berberian

1

Christiane Hopker

1

Ingrid Mazzarotto

1

Jenane Cunha

1

Ana Cristina Guarinello

1

Giselle Massi

1

Ana Crippa

2

1_{Masters and Doctorate Program in Communication Disorders,}

Universidade Tuiuti do Paraná, Curitiba, Paraná, Brazil

2_{Department of Neurophysiology, Universidade Federal do Paraná,}

Curitiba, Brazil

Int Arch Otorhinolaryngol 2015;19:302–308.

Address for correspondence Ana Cristina Guarinello, PhD, Masters and Doctoral Program of Communication Disorders, University Tuiuti of Paraná, Alexandre Eduardo Klat, 66 casa 2, Curitiba 82130-120, Brazil (e-mail: acguarinello@gmail.com).

Introduction

About 50 million people suffer from epilepsy with active seizures and 30% of them have refractory epilepsy (i.e., no response to properly conducted drug treatment).1 Temporal lobe epilepsy (TLE) is the most common form of epilepsy in adults. It is speciﬁc, with a high level of incidence and severity, and is characterized by the presence

of simple and complex partial seizures. The temporal lobe can be divided into medial (playing an important role in episodic and autobiographical memory, coding, and temporal ordering of events in verbal memory, and visuospatial memory) as well as neocortical (related to semantic memory).2

Temporal lobectomy controls seizures in up to 70% of refractory epilepsy cases, but when found in the left

Keywords

► epilepsy

► language

► reading

► speech-language and

hearing sciences

Abstract

Introduction

About 50 million people have epilepsy and 30% of them have epilepsy

that does not respond to properly conducted drug treatment.

Objective

Verify the incidence of language disorders in oral language, speech, and

written language of subjects with dif

ﬁ

cult to control temporal lobe epilepsy (TLE) and

compare the occurrence of these disorders in subjects before and after surgery.

Methods

Cross-sectional study with quantitative analysis, exploratory type. A

ques-tionnaire for data collection was administered covering the following aspects: oral

language, speech complaints, and writing production and comprehension. Criteria for

inclusion of subjects were a diagnosis of TLE refractory to drug treatment and at least

4 years of schooling.

Results

The sample of 63 patients with TLE was divided into two groups: presurgical

(

n

¼

31) and postsurgical (

_n

¼

32). In the postsurgical group, there was a higher

frequency of left lobectomy (75%) than right (25%).

Conclusion

Statistical analysis was performed with the chi-square test (signi

ﬁ

cance

level of 0.05). Complaints related to speech-language attention were more

predomi-nant in postsurgical subjects. Analysis of oral language, speech, and written language in

subjects with epilepsy who underwent temporal lobectomy or not showed

ﬁ

ndings

consistent with symptoms related to transient aphasia, with the presence of

para-phasias, as well as changes in speech prosody and melody. These symptoms appeared

more associated with recurrence after having a temporal lobectomy.

received

December 10, 2014 accepted

January 26, 2015 published online March 10, 2015

DOI http://dx.doi.org/ 10.1055/s-0035-1547524. ISSN 1809-9777.

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hemisphere, it can impair oral language functions, espe-cially related to naming.3Diminishment in verbal memory is also reported as a common effect after surgery on the dominant hemisphere of the temporal lobe.4–7 _Studies

show that patients who undergo temporal lobectomy may present de_ﬁcits in semantic access in some tasks using work recovery.8Examining the efﬁciency of lexical and semantic processing, in association with the activation of the brain, one realizes that a temporal lobectomy is associated with a failure in the functional organization of cortical networks involved in lexical and semantic processing.9

The resection of the temporal lobe can bring risks to verbal and visual episodic memory, as well as naming. Studies have reported declining naming and semantic functions postoperatively, suggesting the hypothesis that naming deﬁcits arise from the functional specialization of the left temporal lobe and the semantic interpretation of visual input.10,11Studies pointed to the fact that patients with left resection showed anomia in simple semantic tasks and that with increasing complexity of the task, they showed semantic deﬁcit.5 Studies also have focused on brain reorganization for the processing of oral language during the postsurgical period.3,12,13In the preoperative period, aspects of determining the dominant hemisphere of oral language, which is critical in planning surgical procedures, are being investigated.14

Regarding written language, one study compared reading skills (comprehension and sentence recognition, as well as memory accuracy,_ﬂuency, and complexity) in patients after a left temporal resection with those from a control group.15 Findings showed that, after surgery, proﬁciency in reading remains preserved due to a compensation mechanism of the right hemisphere coupled with integration of activated brain areas in the process.

Although surgical resection is common for the treatment of refractory TLE, the literature dealing with possible changes in oral language, speech, and written language in patients undergoing temporal lobectomy is scarce, a factor that jus-tiﬁes this study.

Considering the multidimensional impacts of epilepsy, including those that are linguistic and psychological, this study aims to verify the incidence of language disorders in oral language, speech, and writing language in subjects with TLE that is difﬁcult to control and compare the occurrence of these disorders before and after surgery.

Methods

This is a cross-sectional, quantitative, exploratory study con-ducted in the Adult Epilepsy Clinic. This integrated epilepsy care program is a referral center in the Public Health System in Brazil and serves patients referred from various regions of the country. Clinic consultations occur in two stages: presur-gical and postsurpresur-gical monitoring (40 consultations per

month) and intractable epilepsy patients (180 consultations

per month).

Evaluation

For data collection, a questionnaire with open and closed questions was given to subjects by a nurse and a speech therapist, averaging 30 minutes in duration. After that, a speech-language therapist applied a speech-language evalu-ation. Both tools have questions encompassing speech com-plaints, as well as speech and writing for both production and comprehension. Inclusion criteria for the study were having a diagnosis of refractory TLE (i.e., no response to properly conducted drug treatment) and at least 4 years of schooling. Patients who did not properly follow drug treatment or medical management were excluded. The questionnaire was answered after reading and signing the consent form.

Participants

The sample was comprised of 63 patients with TLE divided into two groups: presurgical (PRE-CIR;n¼31) and

postsur-gical (POS-CIR;n¼32). The PRE-CIR group was composed of

20 female (64.5%) and 11 male (35.5%) subjects with mean age of 40.4 years (standard deviation 12.7). In this group there was a higher prevalence of left TLE (n¼14), followed by right

TLE (n¼9) and bilateral TLE (n¼8). The POS-CIR group was

composed of 15 female (46.9%) and 17 male (53.1%) subjects, with mean age of 39.7 years (standard deviation 9.6). In this group there was a predominance of left TLE (n¼14),

fol-lowed by right TLE (n¼9) and bilateral TLE (n¼8). There

was a higher frequency of left lobectomy, 75% (n¼24), with

right making up 25% (n¼8). The time interval between the

temporal lobectomy and data collection ranged from 1 to 39 months.

Analysis

Statistical analysis was performed by applying the chi-square test (signiﬁcance levelp<0.05).

Ethics

The project was approved by the Ethics Committee registra-tion number 380977, CAAE: 18218413.9.0000.0096 of Sep 9, 2013.

Results

Of the total respondents, 68% presented with one or more aspects of interest to speech-language pathology and 62% had a change in the area of language. The aforementioned com-plaints were related to chewing, swallowing, hearing, vestib-ular system, and voice (►Table 1).

Using the chi-square test, the POS-CIR group presented a more signiﬁcant proportion of speech-language pathology complaints.

In the POS-CIR group, chewing alterations were more frequent, with 25% describing difﬁculty in opening their mouth (lasting 1 to 3 months after surgery). With swallowing, 6.2% reported pain for20 days postoperatively. Tinnitus, ear

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Frequent changes to speech production were speech rate (12.6%), prosody (8%), and speech intelligibility (8%). When comparing PRE-CIR and POS-CIR groups using the chi-square test, there was a signiﬁcant difference only for the speech rate, with an appropriate speed being better among PRE-CIR subjects (►Table 2). For the application of the test, the

following variables were considered: phonological aspects, speech rate, prosody, as well as discourse understanding and structure.

To analyze possible changes in oral language related to the surgical procedure, pre- and postprocedure complaints (for POS-CIR) and current complaints (for PRE-CIR) were investi-gated. The subjects’responses were forgetting and missing words, anomia, paraphasia, memory loss, and stuttering

(►Table 3). Regarding these aspects, no signiﬁcant differences

between groups were observed. It is noteworthy that for application of the test, answers of none and no complaint were considered.

From the perception of the subjects, alterations and/ or improvements in oral language and speech production and comprehension after surgery (POS-CIR) were investigated. The answers were classiﬁed as forgetting and missing words, anomia, paraphasia, memory loss, worsening of preexisting symptoms of stuttering/speech/memory, and difﬁculty in articulation (►Table 4).

Of the total POS-CIR subjects, 53% of participants reported some disorder. The most frequent complaints were forgetting and missing words (25%), paraphasia (12.5%), and worsening of preexisting symptoms of stuttering, speech, and memory (12.5%).

On the patient’s perception of improvement in oral lan-guage and speech, after surgery, 12.5% reported feeling increased competence to speak and improvement in their emotional state to talk.

The relationship between oral language and speech dis-orders and surgery was not statistically signiﬁcant, although a higher incidence of alterations was observed in patients with left TLE (►Table 5).

Through the chi-square test, there was no signiﬁcant difference in any case. To implement the test we considered the response categories: phonological aspects (omissions and

distortionsþsubstitutions), speech rate (adequate and fast þslow), prosody (adequate and monotone).

Results related to the reading and writing results are described in►Table 6. There were no statistically signiﬁcant

differences between groups related to written language; however, the PRE-CIR group showed a higher percentage of disorders, with 16.1% in reading comprehension and 12.9% in writing production.

Regarding disorders after surgery, 6.2% of participants reported difﬁculties related to the formal aspects (spelling) and 6.2% had dif_ﬁculties understanding the written text.

Discussion

Complaints related to speech-language pathology were more predominant in POS-CIR subjects. It can be inferred that complaints related to chewing, swallowing, and hearing can be caused by the surgical procedure because the temporo-mandibular joint is composed of an articulating area whose concave depression lies in a portion of the temporal bone, an area manipulated during the lobectomy procedure, and is also in close proximity to the auditory system. Complaints regard-ing vocal ability may be related to the endotracheal or tracheal intubation procedure used for auxiliary support in artiﬁcial ventilation.

As for speech, the comparison between the POS-CIR and PRE-CIR groups showed statistically significant differences only for the alteration in rate of speech in the POS-CIR subjects. No studies that indicate similarfindings were found. There are references in the literature to the problems of speech production, as well asfindings of our study, on the correlation between epilepsy and changes in prosody.16 In addition, regarding oral language, both groups presented alterations as missing words, anomia, paraphasia, memory loss, and stuttering.

According to the literature, it appears that TLE has been associated with such alterations because the epileptogenic zone is located in the temporal lobe dominant for such functions. And TLE is also associated with dysfunction in memory when it involves the temporal lobes of both hemi-spheres.17 The occurrence of symptoms classiﬁed as

Table 1 Distribution of the sample according to speech-language pathology complaints

Complaints Groups p

POS-CIR (n¼32) PRE-CIR (n¼31)

None 15 (46.9%) 28 (90.3%) 0.0001

Chewing 8 (25.0%) –(0.0%)

Swallowing 2 (6.2%) 1 (3.2%)

Hearing 7 (21.9%) 2 (6.4%)

Vestibular system 1 (3.1%) –(0.0%)

Voice 1 (3.1%) –(0.0%)

Abbreviations: POS-CIR, after frontal lobotomy; PRE-CIR, before frontal lobotomy.

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Table 2 Distribution of the sample according to aspects of oral language and speech

Groups p

I—Speech production

Articulation 0.1572

Adequate 30 (93.8%) 31 (100%)

Blocked 2 (6.2%) –(0.0%)

Phonological aspects 0.1572

Adequate 30 (93.8%) 31 (100%)

Omissions 1 (3.1%) –(0.0%)

Distortions –(0.0%) –(0.0%)

Substitutions 1 (3.1%) –(0.0%)

Unintelligible speech 0.1734

Not compromised 28 (87.5%) 30 (96.8%)

Slightly compromised 4 (12.5%) 1 (3.2%)

Speed of speech 0.0263

Adequate 25 (78.1%) 30 (96.8%)

Fast 2 (6.2%) –(0.0%)

Slow 5 (16.6%) 1 (3.2%)

Prosody 0.1617

Adequate 27 (84.4%) 30 (96.8%)

Monotone 4 (12.5%) 1 (3.2%)

Inconclusive 1 (3.1%) –(0.0%)

II—Comprehension and structuring of oral language

Comprehension 0.5354

Not compromised 31 (96.9%) 29 (93.5%)

Structuring 0.572

Present 30 (93.8%) 31 (100%)

Partial 2 (6.2%) –(0.0%)

Chi-square, signiﬁcance level of 0.05.

Table 3 Distribution of the sample according to oral language

Complaints Groups p

Pos-CIR (n¼32) Pre-CIR (n¼31)

None 24 (75.0%) 18 (58.1%) 0.2414

Forgetting and missing words 6 (18.8%) 3 (9.7%)

Anomia 1 (3.2%) 4 (12.9%)

Paraphasias –(0.0%) 2 (6.4%)

Memory loss –(0.0%) 5 (16.1%)

Stuttering 5 (15.6%) 2 (6.4%)

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forgetting and missing words are frequently reported by patients with TLE.18,19

In our study, we found that paraphasias corroborated another study in which, after having a temporal lobectomy, patients identiﬁed deﬁcits in semantic retrieval tasks with words, showing paraphasias.8

Naming difficulties also were described in the literature after left temporal lobe surgery.3,20,21Naming deficits were observed only in patients with left TLE and yet a signi_ficant association was found between the decline of postoperative naming and prejudice to semantic functions.11Naming has been identi_fied in regions of the cortex involved in oral language. Studies show that patients with TLE have no difficulty in naming concrete objects that were visually presented to them. However, before and after surgery, they often show difficulty infinding words in their daily activities (forgetting/missing words, anomia).22

Table 4 Distribution of sample according to postsurgery oral

language and speech complaints (n¼₃₂₎

Complaint Frequency (%)

None 15 (46.9%)

Forgetting and missing words

8 (25.0%)

Anomia 3 (9.4%)

Paraphasia 4 (12.5%)

Worsening of memory

3 (9.4%)

Worsening of stut-tering, speech, and memory

4 (12.5%)

Difﬁculty articulating

1 (3.1%)

Table 5 Relationship between aspects of speech and oral language and surgery side

Side of surgery p

Left (n¼₂₄₎ _{Right (n}¼₈₎

I—Speech production

Articulation

Adequate 22 (68.8%) 8 (25.0%) 0.3991

Blocked 2 (6.2%) –(0.0%)

Speech-language aspects

Adequate 22 (68.8%) 8 (25.0%) 0.3991

Distortions 1 (3.1%) –(0.0%)

Substitutions 1 (3.1%) –(0.0%)

Unintelligible speech

Not compromised 21 (65.6%) 7 (21.9%) >0.9999

Speed of speech

Adequate 18 (56.2%) 7 (21.9%) 0.4589

Fast 2 (6.2%) –(0.0%)

Slow 4 (12.4%) 1 (3.2%)

Prosody

Adequate 21 (65.6%) 6 (18.8%) 0.9013

Monotone 3 (9.4%) 1 (3.1%)

Inconclusive –(0.0%) 1 (3.1%)

II—Comprehension and structuring of oral language

Comprehension

Not compromised 23 (71.9%) 8 (25.0%) 0.5575

Slightly compromised 1 (3.1%) –(0.0%)

Structuring

Present 23 (71.9%) 7 (21.9%) 0.3991

Partial 1 (3.1%) 1 (3.1%)

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As with the_ﬁndings of this study, previous research found that TLE is associated with alterations to the functioning of episodic long-term memory, and recovery processes and imme-diate recognition (short-term memory) appear less affect-ed.23–25 _{The effect of epilepsy on memory and forgetting}

words is better understood in mesial TLE with hippocampal sclerosis, because the hippocampus and entorhinal cortex neigh-bors are involved in the formation of declarative memory. As the verbal episodic memory is strongly associated with the domi-nant hemisphere, patients with left mesial TLE, in general, exhibit deﬁcits in consolidation and recovery of verbal memory. In cases where the epileptic focus is located in the nondominant hemisphere, visuospatial memory may be affected.26

One study demonstrated the link between problems with long-term memory and TLE, because the mesial temporal lobe plays a prominent role in memory.27Subjects with TLE tend to show amnesic alterations.28Other aspects of amnesic function may be factors such as remote, autobiographical, and semantic memory.29

Most participants still hadﬂuent reading skills and com-prehension, and there was no signiﬁcant difference between PRE-CIR and POST-CIR in aspects of reading and reading comprehension, which corroborates with the literature.15A higher occurrence of changes related to reading comprehen-sion and written production was cited by the PRE-CIR group, corroborating prior studies.30,31

Conclusion

In the analysis of aspects of oral language, speech, and written language, subjects with epilepsy who did or did not undergo a temporal lobectomy showed ﬁndings consistent with the symptoms related to transient aphasia, with the presence of paraphasias, as well as changes in speech prosody and melody. These symptoms are peculiar and appear with higher frequency when associated with temporal lobectomy surgery. The study highlighted the need to implement research that addresses implications in speech and written language sci-ences for people with epilepsy.

References

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Table 6 Distribution of the sample according to aspects of reading and writing

Written Language Groups p

Reading

Fluent 2 (87.5%) 25 (80.6%) 0.4567

Fluency compromised 3 (9.4%) –(0.0%)

Inconclusive 1 (3.1%) 1 (3.2%)

Doesn’t read –(0.0%) 5 (16.1%)

Reading comprehension

Yes 29 (90.6%) 23 (74.2%) 0.0695

No 1 (3.1%) 5 (16.1%)

Inconclusive 2 (6.2%) 3 (9.7%)

Reading and writing complaints

None 31 (96.9%) 26 (83.9%) 0.0788

Severe difficulties or impossible in writing 1 (3.1%) 4 (12.9%) Severe difficulties or impossible in reading –(0.0%) 1 (3.2%) Written language notification post surgery

None 28 (87.5%) –(0.0%)

Orthographic aspects 2 (6.2%) –(0.0%)

Semantic aspects in reading 2 (6.2%) –(0.0%)

Semantic aspects in writing 1 (3.1%) –(0.0%)

Illiterate 1 (3.1%) –(0.0%)

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